Disruption of Locomotion in Response to Hindlimb Muscle Stretch at Acute and Chronic Time Points after a Spinal Cord Injury in Rats

Abstract

After spinal cord injury (SCI) muscle contractures develop in the plegic limbs of many patients. Physical therapists commonly use stretching as an approach to avoid contractures and to maintain the extensibility of soft tissues. We found previously that a daily stretching protocol has a negative effect on locomotor recovery in rats with mild thoracic SCI. The purpose of the current study was to determine the effects of stretching on locomotor function at acute and chronic time points after moderately severe contusive SCI. Female Sprague-Dawley rats with 25 g-cm T10 contusion injuries received our standard 24-min stretching protocol starting 4 days (acutely) or 10 weeks (chronically) post-injury (5 days/week for 5 or 4 weeks, respectively). Locomotor function was assessed using the BBB (Basso, Beattie, and Bresnahan) Open Field Locomotor Scale, video-based kinematics, and gait analysis. Locomotor deficits were evident in the acute animals after only 5 days of stretching and increasing the perceived intensity of stretching at week 4 resulted in greater impairment. Stretching initiated chronically resulted in dramatic decrements in locomotor function because most animals had BBB scores of 0-3 for weeks 2, 3, and 4 of stretching. Locomotor function recovered to control levels for both groups within 2 weeks once daily stretching ceased. Histological analysis revealed no apparent signs of overt and persistent damage to muscles undergoing stretching. The current study extends our observations of the stretching phenomenon to a more clinically relevant moderately severe SCI animal model. The results are in agreement with our previous findings and further demonstrate that spinal cord locomotor circuitry is especially vulnerable to the negative effects of stretching at chronic time points. While the clinical relevance of this phenomenon remains unknown, we speculate that stretching may contribute to the lack of locomotor recovery in some patients.

Stretching adversely modulates locomotor capacity following spinal cord injury via activation of nociceptive afferents.

“…As in previous studies, these animals achieved some locomotor recovery over the weekends when they were not stretched. [186,218] However, one stretching session (Monday morning) was enough to again reduce the BBB scores to below 4 ( Fig.1). Lack of hindlimb movement was further confirmed with the more objective kinematic and gait analysis.…”

“…Contrary to our hypothesis, dynamic stretching dramatically disrupted locomotor function reducing BBB scores to levels similar to those of static stretching even though the total amount of stretch that the animals received on a daily basis was less (20 seconds less/stretch) than in our previous studies. [186,218] Histological analysis of the muscles revealed that for the ankle extensor MG the group sacrificed two hours after stretching had elevated numbers of centralized nuclei (8%) as compared to the rats sacrificed four weeks later (~4%)…”

“…1) or any of our earlier studies. [218] However, in the second week of stretching, one session does cause the deficits, presumably due to the sensitization of afferents.…”

“…[191] Locomotor function was assessed at least weekly using the BBB Open Field Locomotor Scale [187] and video-based kinematic and gait analysis was done biweekly. As described previously, [218] we used a 3 segment, 2 angle model of the hindlimb and "joint" excursions were measured as the hip-ankle-toe (HAT) and iliac cresthip-ankle (IHA) angles. Two gait indices were also used, the regularity index (RI) and the plantar stepping index (PSI) based on ventral-view video allowing paw placement order, timing and location to be determined for every step taken (from initial contact to lift-off)…”

“…[188] At six weeks post injury the animals entered a four week dynamic stretch protocol that was performed 5 days a week for 4 weeks. Dynamic stretching consisted of the same six bilateral stretches of major hindlimb muscle groups as our previous static stretching protocol, [171,218] however, instead of holding the limb at the end ROM of each stretch for 1 min, each stretch was held for only 2 seconds, followed by a 1 second release, repeated 20 times over a one minute period. A metronome (at 1Hz) was set to the 2-1 ratio, using different tones, in order to give an audible clue to the rat physical therapists (PT) allowing them to maintain the rhythm and ensuring that timing was consistent and accurate between therapists for each animal every day.…”